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Eastern Slate Pencil Urchin
Phyllacanthus parvispinus (Tennison-Wood 1879)
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Hannah McQuitty 2015
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Summary | |
Phyllacanthus parvispinus is a sea urchin found in rocky reefs along the east Australian coastline. They are commonly referred as the Eastern Slate Pencil Urchin, the term coined by their diagnostic thick, blunt grey spines. These thick spines are characteristic of the order Cidaroida and are used as their primary mode of locomotion. The test is deep red in colour and often grow to about 50-60mm. P.parvispinus actively seeks shade, hiding in crevices during the day and grazing nocturnally. They feed on algae using their specialised feeding structure known as Aristotle’s lantern. A short histological comparative study was conducted observing the morphological differences in podia of P.phyllacanthus with other species of echinoid including Tripneustus gratilla, Echinometra mathaei and Centrostephanus rodgersii. It was observed that the suckered ends of podia of P.parvispinus were smaller and less defined, making them inefficient for locomotion. This is most likely an adaptation for using their primary spines as their main locomotory organs.
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| Figure 1 |
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Physical Description |
General Echinoid Bauplan | |
There are two major morphological groupings within Echinoidea: the regular urchins and the irregular urchins. Regular urchins comprise what are commonly recognised as sea urchins, with a spherical body and long, movable spines (Ruppert & Barnes, 1994). They exhibit pentaradial symmetry.The fusing and suturing together of the skeletal ossicles into a solid test distinguishes echinoids from other echinoderm classes. The test is then divided into ten radial sections which converge at the oral and aboral poles (refer Figure 2) (Ruppert & Barnes, 1994). Five of these comprise the ambulacral areas which contain podia while the remaining five bereft of tube feet are called the interambulacral areas (Ruppert & Barnes, 1994). The mouth is situated toward the substratum. It contains five, calcerous teeth that make up a specialised feeding structure known as Aristotle's lantern. Surrounding the mouth is the peristomial membrane and modified, buccal podia (refer Figure 2).The periproct makes up the aboral region. It included five radially arranged genital plates and the madreporite.
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| Figure 2 |
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Pedicellariae | |
Pedicellariae are present all over the body. They are defined as a pair of jaws surmounted onto a stalk attached to a small tubercle on the test by a ball-and-socket like joint. Muscles at the base of the stalk are used to elevate and direct the pedicellariae, usually in response to stimuli (Lawrence, 1987; Ruppert & Barnes, 1994).There are different morphological forms of pedicellariae in echinoids: cidaroids possess globiferous pedicellaria and tridentate pedicellaria (Lawrence, 2013). The pedicellariae can be used for a variety of functions including cleaning, defence, biting (Ruppert & Barnes, 1994).
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Spines | |
Phyllacanthus parvispinus is easily identified by its thick, blunt spines which are arranged in a pentamerous manner (refer Figure 3). Primary spines are situated ventrally and have been observed to be 5-6cm in length. P.parvispinus is distinguished by their 8 primary spines, whereas other species within the genus such as P.dubia and P.imperialis only possess 6 (Tennison-Wood 1879). A single primary spine is located on each interambulacral plate (Lawrence, 2013). The number of these primary tubercles is constant regardless of age, sex or condition (Tennison-Wood, 1879). Unlike other echinoids, members of Cidaroida lack an epidermis on the primary spines and have an external cortex (Lawrence, 2013). Surrounding the peristomial opening are much smaller and narrower spines which are deep red in colour known as miliaries. These are condensed much closer together and are more abundant in numbers (refer figure 4). Primary spines are gray while juvenile spines are mid to deep red.
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| Figure 3 |
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| Figure 4 |
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Test | |
The main body is termed the test and is a deep maroon in colour. The test is elevated from the ground by the spines and has a dorso-ventral axis with the oral surface toward the bottom and aboral side exposed to the water column (Tennison-Wood, 1879). Due to spines being relatively spaced on the interambulacral plates, the test of the organism is rather exposed. Visually, it appears velvety and smooth. Podia were observed to extend from the ventral side exclusively.
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Size | |
The overall body size of P. parvispinus can vary between 10-15cm. Primary spines are around 5-6cm in length while smaller spines vary between 2-4cm.
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Ecology |
Habitat | |
P. parvispinus is commonly found on or near rocky reefs and in intertidal pools of up to 80m in depth. Reduced development and musculature in tube feet reduces their ability for adhesion and locomotion, restricting them to regions of low wave energy and habitats with rugose features (Lawrence, 2013). Their their thick, primary spines to wedge themselves into rock crevices and cavities on shallow reefs for protection from water activity and predation (Lawrence, 2013).
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Symbionts | |
Cidaroids are known for harbouring ectocommensals on or within their primary spines (Lawrence, 2013). The wide study of ectocommensalism on cidaroid spines has suggested that these associations are either species-specific or specific to cidaroids in general. They are not, however, ubiquitous across cidaroid species. No negative effects of ectocommensals has been demonstrated across the literature, although it has been proposed that infestation on primary spines could result in increased drag or exposure to epibiont grazers (Schneider, 2003). It has also been speculated that positive effects of ectocommensals could include camouflage and chemical protection, although neither have been tested (Schneider, 2003).
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Life History and Behaviour |
Locomotion | |
As the food commonly consumed by echinoids does not require rapid movement, locomotion is relatively slow (Lawrence, 1987). Locomotion is adapted for hard and soft substratum, and use either their spines, tube feet or a combination of both for movement. The podia function via pressure in water vascular system causing protraction and uplift (refer to Anatomy and physiology section for more detail) (Boolootian, 1966; Lawrence, 1987). The spines are also used for locomotory function. This requires precise coordination, not only of all tubercles, but also the podia and pedicellariae (Boolootian, 1966).
The podia of Cidaroids have reduced suckers on the ends, impeding their ability to rely on tube feet for locomotion like other echinoids (Lawrence, 1987; Lawrence, 2013). Instead, they use their thick spines for movement but is done so with considerable dexterity (Lawrence, 1987).
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Video showing P.Parvispinus using spines for locomotion. Tube feet are visible from underside of test. Video by Hannah McQuitty.
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Behaviour | |
P.parvispinus, like other cidaroids, tend to be negatively phototropic. They seek shade in crevices during daylight and are nocturnal grazers (Boolootian, 1966).
When observing P.parvispinus in the laboratory, it appeared to react to the disturbance of being handled. It would become quite active and move relatively quickly. The behavior contrasted to what was observed when the individual was among reef rubble in the laboratory aquarium.
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Feeding | |
Echinoids are omnivorous and tend be generalist feeders (Ruppert & Barnes, 1994). They are scavengers, predators and grazers, consuming a variety of algae, plants and animals (Lawrence, 2013). The presence of specialized feeding structure, Aristotle’s Lantern, allows for versatile feeding techniques such as grazing, rasping and tearing as well as increasing the variety of food available (Lawrence, 2013). Grazing occurs by scraping the substratum with the five teeth within Aristotle’s lantern. A more detailed description of the feeding apparatus can be found in the Anatomy and Physiology section of this page.
Within the order Cidaroida, the Aristotle’s lantern is considered more primitive with its feeding technique restricted to the opening and closing of the teeth. Higher groups are able to swing the lantern laterally (Ruppert & Barnes, 1994). The diet of cidaroids varies with habitat. Gut contents of soft bottom dwelling cidaroids have been found to contain formaniferans, bryozoans, sponges and particles. Cidaroids also feed on hard surfaces such as coral rock, scouring it clean of algae and leaving marks on the rock surfaces
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Reproduction | |
Regular echinoids, including P.parvispinus, are dioecious. The gonads are located on the inner side of the test, suspended along the interambulacral grooves above the lantern. Each gonad extends into a short gonoduct and opens externally through a gonopore located on each genital plate (Boolootian, 1966; Ruppert & Barnes, 1994). Spawning of can be either broadcast or spermcast with some species brooding fertilized eggs. The brooded eggs are retained on the peristome or periproct, held into place using their spines (Boolootian, 1966). The breeding season of P.parvispinus is between February and March annually.
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Development | |
Echinoids are deuterostomes and demonstrate radial cleavage. Within 12 hours of fertilization, the blastula metamorphoses into a ciliated, free-swimming larva. Gastrulation then occurs and the blastula develops into the echinopluteus: a planktonic larvae which bears six pairs of larval arms (refer Figure 5). The skeleton begins to form later in the larval stage, beginning with the five genital plates and then the ocular. The echinopluteus gradually sinks to the benthos and undergoes rapid development into adult form (Ruppert & Barnes, 1994).
A variety of developmental modes are observed in the cidaroids such as brooding, lecithotrophy and planktotrophy (Lawrence, 2013). Phyllacanthus parvispinus in particular displays pelagic lecithotrophic larvae, relying on their yolk supply as their main food and energy source (Parks et al., 1986). Like other cidaroids, they lack the development of a vestibule. A feature that differs from other cidaroids is the direct development observed in P.parvispinus larvae. Direct development is characteristic of the euechinoids, which P.parvispinus shares other common features with as such as larger gametes, an equal fourth cleavage, a wrinkled blastula and accelerated development of the adult rudiment (Parks et al., 1986). These variations are most likely functional modifications due to the different developmental mode.
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| Figure 5 |
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Anatomy and Physiology |
Internal Structure | |
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| Figure 6 |
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Aristotle's Lantern | |
Aristotle’s lantern is a specialised musculoskeletal system found exclusively in echinoids (refer Figure 7). It is comprised of five radially arranged, calcareous plates called pyramids. A long, calcareous band passes through the middle of each pyramid where a hard, pointed tooth projects beyond the tip of the pyramid. This results in five pointed teeth at the oral end of the lantern (Lawrence, 2013; Ruppert & Barnes, 1994). The upper end of the calcareous band is enclosed in a dental sac and is the site of new tooth formation. Smaller, rod-like pieces are also found at the aboral end of the lantern. Each pyramid is connected to the the edge of the test via five pairs of retractor muscles (Lawrence, 2013). These are responsible for retraction as well as opening the jaw. Interpyramidal muscles are used to pull the jaws back together. This gives rise to the ability to rip, tear and scrape food (Ruppert & Barnes,1994).
Aristotle's lantern is slightly modified in cidaroids. The lantern is considered more primitive as they are not capable of protruding or swinging the lantern but can only open and close the jaws. This makes the lantern less efficient and limits their feeding behaviour and preferences (Lawrence, 2013).
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| Video showing the opening and closing motion of Aristotle's lantern of P.parvispinus. Video by Hannah McQuitty. |
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| Figure 7 |
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Digestive System | |
Food enters the mouth though Aristotle’s lantern where it is then transported to the buccal cavity and the pharynx. The esophagus then descends along the outer side of Aristotle’s lantern joining with a tubular stomach. At this junction, a broad cecum is present in all other groups of echinoids excluding the Cidaroids (Lawrence, 2013). The stomach circles its way around the test, passing into the aborla intestine which also circles the test in the opposite direction (refer Figure 6). The intestine ascends to meet the rectum and anus within the periproct.
Cidaroids are the only order of within the Echinoidea that do not possess a siphon but rather a siphonal groove which runs along the margin of the stomach (Lawrence, 2013).The inner epithelium is ciliated, producing a current to help move water in the groove along the side of food mass in the stomach (Lawrence, 2013).
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Nervous System | |
The echinoid nervous system is centered around a circumoral nerve ring which encircles the pharynx and lantern. Radial nerves run along the underside of the test below the radial canals of the water vascular system. There are numerous sensory cells located in the epithelium, spines, pedicellariae and podia of echinoids which make up the majority of the sensory system (Ruppert & Barnes, 1994). Statocysts are located within spheridia along the ambulacral grooves.
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Gas Exchange, Internal Transport and Excretion | |
Regular echinoids possess five pairs of peristomial gills which are important sites of gas exchange. They are outpocketings of the body wall, highly branched and lined internally and externally with a ciliated epidermis (Ruppert & Barnes, 1994). The coelom pumps coelomic fluid in and out of the the gills using a system of muscles and ossicles associated with Aristotle’s lantern. Podia are also play a role in gas exchange. It is common in echinoids for the most aboral podia to be modified specifically for this function to increase gas exchange. These podia are usually not used in locomotion and may lack suckers. Two-way circulation of fluid occurs in the septate podia and ampullae (refer Figure 8). The physical separation of the opposing fluid streams in the septa reduces the diffusive loss of oxygen from the incoming oxygen rich stream to the outgoing oxygen depleted stream (Ruppert & Barnes, 1994).
A specific feature of Cidaroid respiration is the presence of the Stewart’s organs, which occur only in the Cidaroida and Echinothuroidea (refer Figure 7) (De Ridder, 1988). They are bush-shaped diverticulae which protrudes from the roof of the peripharyngeal cavity above Aristotle’s lantern, lined with ciliated epidermis (Lawrence, 2013). Due to their close proximity to the ambulacral ampullae, they provide oxygen to the peripharyngeal cavities and the muscles within Aristotle’s lantern (De Ridder, 1988).
The circulatory system of echinoids relies on the coelomic fluid to transport nutrients and gases around the body. They also possess a well developed hemal system (Ruppert & Barnes, 1994). Coelomocytes are used in excretion to carry particulate waste. Excretion occurs at the aboral end near the axial organ.
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| Figure 8 |
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Water Vascular System | |
Echinoids, like all other echinoderms, possess a water vascular system (WVS) is fluid filled canal system which plays a role which in locomotion, respiration, feeding and internal transport. It is a tubular system derived from the coelom thus the canals are lined with ciliated epithelium (Nichols, 1979; Ruppert & Barnes, 1994). It is a hydraulic system which applies a series of pressure gradients to hundreds of podia, resulting in their locomotor ability.
It consists of a central ring vessel that encircles the esophagus just above the lantern, from which a an axial tube ascends to the exterior of the organism.This is called the madreporite and is the site where water enters WVS via the action of cilia (Ruppert & Barnes, 1994). It is located on one of the five genital plates of echinoids (Nichols, 1974). A structure called the stone canal, a structure that adds calcareous deposits and structure to the walls, then descends to merge with the ring canal. From the ring canal extends five radial canals which ascend along the inside of the test in the ambulacral areas (Ruppert & Barnes, 1994). Each radial canal finishes with a small tentacle called the terminal tentacle which protrudes from the most apical ambulacral plate (Ruppert & Barnes, 1994). Lateral canals extend from each radial canal, connecting the podia and ampullae, and penetrate the ambulacral ossicles to the exterior of the organism. This contrasts other echinoderms whose radial canals pass between the ambulacral ossicles. The lateral canals comprise of an ampulla, a small muscular sac that extends down to the podium (tube foot) which is exposed through the test to the water column (Ruppert & Barnes, 1994).
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Podia | |
The podia of echinoids play an important role in locomotion thus powerful postural bending and movement is required. The protraction of the podia is caused mainly by the retractor muscles which work against the pressure of the fluid produced by the ampulla and, to a lesser extent, by specialised muscles at the head of the podium (Nichols, 1979). When the ampulla contracts, water is forced into the tube foot which elongates, coming into contact with the substratum and adhering (Ruppert & Barnes, 1994). The podium then detaches from the substratum. The repetition of this action across hundreds of tube feet result in the locomotion of echinoids and other echinoderms.
Within the echinoids, the greatest radiation of tube feet is observed (Nichols, 1979). All tube feet extended from the test bear a sucker at the distal end. This is excluding tube feet surrounding the peristomial area which lack a sucker. Unlike asteroids, there is a calcite skeleton which is composed of the rosette, several pieces arranged radially around the lumen, and the frame, smaller ossicles proximal to the rosette (Nichols, 1979). Situated around the lumen is a sensory ring.
The podia of Phyllacanthus parvispinus is shown extended in Figure 9. They were mainly observed on the underside of the test.
Short investigation: Histological comparison of podia in Cidaroid and Euechinoid species.
The podia of echinoids often play a role as locomotory organs. Order Cidaroida, also known as the pencil urchins, rely on their thick spines for movement. P.parvispinus is an example of this type of locomotion. While tube feet are extended during movement of the organism, all locomotory effort is conducted by the spines. With this in mind, I decided to compare the podia of P.parvispinus to other euechinoids species who use tube feet as their primary means of locomotion. It was predicted that there will be less musculature and complexity in podia of P.parvispinus compared to that of other euechinoids.
Samples of the tube feet were taken from the echinoids Phyllacanthus parvispinus, Tripneustus gratilla, Echinometra mathaei and Centrostephanus rodgersii, the former three representative of the euechinoids. The samples were fixed in 4% paraformaldehyde fixative in a MOPS fixation buffer (4%PFA). To make features easier to observe under light microscopy a clearing agent was used. First the specimens were transferred to a solution of 50% fixative and 50% ethanol to remove the remaining fixative. They were then transferred to a 200µl 70% ethanol solution and left for five minutes. Lastly, they were transferred to 100µl solution of glycerol which acted as the clearing agent. Methods for this study were adapted from Vickery and McClintock (2000).
There were clear differences in the morphology and structure of the podia when observed under light microscope. P.parvispinus was evidently much smaller in diameter and length compared to the other specimens (refer Figure 10). The sucker on the distal end of the podia is small and inconspicuous, and does not extend laterally from the edge of the stem. In contrast, the sucker of the T.gratilla specimen shows clear projection and definition from the stem of the podium. The end of the sucker was scalloped. The podium is also much larger in diameter and length. The lumen of the the water vascular system is not clearly defined. The C.rodgersii specimen had a well defined lumen in the centre of the tube foot (refer Figure 10). However, the suckered end appeared to be less defined from edges of the stem yet large in size in relation to the stem diameter. The E.mathaei tube foot showed similar scalloping of the sucker to the T.gratilla tube foot. It also had the widest diameter across all species.
The most striking observation between the podia of P.parvispinus and the podia of T.gratilla, E.mathaei and C.rodgersii was the small, poorly defined sucker at the distal end of the tube foot. The suckers of the euechinoid species were clear projections from the stem and lumen, with scalloped/folding of the edge perhaps indicating increased sensory epithelium and musculature (Nichols, 1961).The reason for these differences in morphology most likely relates back function of the tube feet. P.parvispinus is part of the order Cidaroida, the group of echinoids considered the most primitive. Contrary to the euechinoid species discussed, they do not depend on their suckered tube feet for locomotion but primarily on their spines. During movement, the tube-feet act as anchors thus exerting their force perpendicular to the test (Nichols, 1961). This differs in the euechinoids who rely on the bending and protraction of their tube feet as their primary locomotion. It has also been noted that the small size of cidaroid tube feet has made them weak and inefficient, which is possibly the cause for the lack of defined musculature and suckered end observed in P.parvispinus (Lawrence, 2013).
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| Figure 9 |
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| Figure 10 |
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| Figure 11 |
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Evolution and Systematics | |
P. parvispinus is grouped within the phylum Echinodermata based on several phylum-specific traits such as pentaradial symmetry, modified ossicles, water vascular system, dermal branchiae and pedicellariae (Ruppert & Barnes, 1994). They are the invertebrate phyla to be identified as deuterostomes. It has been hypothesised that echinoderms are derived from a bilaterally symmetrical, enteropneust-like ancestor who gradually adapted to pentaradial symmetry when passing through an intermediate pterobranch-like stage. Shortening of the body length but widening in diameter resulted in hydraulic outgrowths from the central coelomic cavity, now identified as pentaradial arms (Gudo, 2005). The echinoderms have a rich fossil history that dates back to the Cambrian (Zamora & Rahman, 2014).
P. parvispinus is further classified into the subphylum Echinozoa which categorises fundamentally globoid taxa who never develop arms (Boolootian, 1966; Ruppert & Barnes, 1994). Their body is predominantly covered in ambulacra and features an aboral anus, periproct and pharynx surrounded by calcareous ossicles. Echinozoa also possess a well-developed hemal system. Within Echinozoa, P. parvispinus is found in the class Echinoidea; taxa with fused tests, strong, movable spines, and pedicellariae. P. parvispinus is then found in the order Cidaroida, which is comprised of primitive sea urchins identified with by thick, blunt spines. Cidaroida are the primitive sister groups to the Euchinoidea, which comprises all other extant echinoids (Lawrence, 2013).
Evolutionary Development
An interesting point to note regarding the evolutionary development of echinoderms is that as larvae, echinoderms are bilaterally symmetrical. The distinctive radial body plan only arises later in the life cycle, in presumptive adult tissue that establish new axes and replaces larval ones. Thus, the development of echinoderms is a pertinent example of not only bauplan transformation during an individual's life cycle, but also of the evolutionary transformation of development from bilaterally symmetrical ancestors (Minsuk et al., 2009).
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| Figure 12 |
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Biogeographic Distribution | |
P.parvispinus is found in the Indo-Pacific Ocean, distributed along the east coast of Australia. They are located predominantly in Queensland and New South Wales, with individuals found in the Great Barrier Reef and Moreton Bay regions. The species is endemic to Australian waters (Davie, 2011).
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| Figure 13 |
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Conservation and Threats | |
IUCN has not listed P.parvispinus as threatened. There appears to be no immediate threats to the species apart from indirect consequences of habitat destruction.
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References | |
Boolootian, R. A. (Ed). (1966). Physiology of Echinodermata. Los Angeles: John Wiley and Sons.
Davie, P. (2011). Wild guide to Moreton Bay and adjacent coasts. Volume 2. South Brisbane: Queensland Museum.
De Ridder, C., Burke, R. D., Mladenov, P. V., Lambert, P., & Parsley, R. L. (1988). Could the Stewart's organs of cidaroid echinoids be internal gills?. InProceedings oh the 6th International Echinoderm Conference. Balkema Publ, 675-681.
De Ridder, C. (1988). Could the Stewart’s organs of cidaroid echinoids be internal gills? In: Burke, R.D., Mladenov, P.V., Lambert, P., Parsley, R.L. (Eds.), Echinoderm
Biology (pp. 675-681). Rotterdam: Balkema Publ.
Gudo, M. (2005). An Evolutionary Scenario For The Origin Of Pentaradial Echinoderms—Implications From The Hydraulic Principles Of Form Determination. Acta biotheoretica, 53(3), 191-216.
Lawrence, J. M. (1987) A functional biology of echinoderms. Maryland: John Hopkins University press.
Lawrence, J. M. (Ed.). (2013). Sea urchins: biology and ecology. Developments in Aquaculture and Fisheries Science, 8, 1-532.
Minsuk, S. B., Turner, F. R., Andrews, M. E., & Raff, R. A. (2009). Axial patterning of the pentaradial adult echinoderm body plan. Development genes and evolution, 219(2), 89-101.
Parks, A. L., Bisgrove, B. W., Wray, G. A., & Raff, R. A. (1989). Direct development in the sea urchin Phyllacanthus parvispinus (Cidaroidea): phylogenetic history and functional modification. The Biological Bulletin, 177(1), 96-109.
Nichols, D. (1961). A comparative histological study of the tube-feet of two regular echinoids. Quarterly Journal of Microscopical Science, 3(58), 157-180.
Ruppert, E.E. & Barnes, R. D. (1994). Invertebrate Zoology 6th Edition. Philadelphia: Saunders College Publishing.
Schneider, C. L. (2003). Hitchhiking on Pennsylvanian echinoids: epibionts on Archaeocidaris. Palaios, 18(4-5), 435-444.
Tenison-Woods, J.E. (1879). On some new Australian Echini. Proceedings of the Linnean Society of New South Wales., 9, 286-287.
The Atlas of Living Australia. (nd). Phyllacanthus parvispinus Tennison-Wood, 1879. Retrieved from http://bie.ala.org.au/species/urn:lsid:biodiversity.org.au:afd.taxon:3926986e-72b8-4c92-a9ed-6dea5bea66e8.
Vickery, M. S., & McClintock, J. B. (2000). Comparative morphology of tube feet among the Asteroidea: phylogenetic implications. American Zoologist, 40(3), 355-364
Zamora, S., & Rahman, I. A. (2014). Deciphering the early evolution of echinoderms with Cambrian fossils. Palaeontology, 57(6), 1105-1119.
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